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Melatonin Receptor (MTNR1A and MTNR2B) Expression During the Breeding Season in the Yak (Bos Grunniens)

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Melatonin Receptor (MTNR1A and MTNR2B) Expression During the Breeding Season in the Yak (Bos Grunniens) Original Paper Czech J. Anim. Sci., 59, 2014 (3): 140–145 Melatonin receptor (MTNR1A and MTNR2B) expression during the breeding season in the yak (Bos grunniens) S.-D. Huo1, 2, R.-J. Long1 1College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, P.R. China 2College of Life Science and Engineering, Northwest University for Nationalities, Lanzhou, P.R. China ABSTRACT: Melatonin plays key roles in a wide range of mammalian body functions, which are mediated by the melatonin-specific cell surface receptor (MTNR1A and MTNR1B). To better understand the role of MTNR in the yak (Bos grunniens), we determined the melatonin receptor mRNA expression level. The analysis showed that the MTNR mRNA expression level was higher in the pineal gland tissue than in the hypothalamus, pituitary gland, and ovary (P < 0.01) during the breeding season. Immunofluorescence analyses showed that yak MTNR was located in the pinealocyte, synaptic ribbon, and synaptic spherules of the pineal gland and that melatonin interacts via nerve fibres. In the hypothalamus, MTNR was located in the magnocellular neurons and parvicellular neurons. MTNR was localized in acidophilic cells and basophilic cells in the pituitary gland. In the ovary, MTNR was present in the ovarian follicle, corpus luteum, and Leydig cells. Keywords: domestic yak; immunofluorescence; MLTR; real-time PCR The domestic yak (Bos grunniens) is a rare bovine receptor 1A (MTNR1A) genes are expressed in the species found at high altitudes in the Qinghai- cumulus-oocytes complex, whereas the MTNR1B Tibetan Plateau and adjacent regions. Yaks have gene is expressed only in the oocytes. Melatonin unique biological and economic characteristics that can enhance the maturation of oocytes in vitro make them resistant to cold. They have evolved a (Berlinguer et al., 2009; Kang et al., 2009; El-Raey et unique body structure and physiological adapta- al., 2011). There was a positive correlation between tion mechanisms. The reproductive mechanism MTNR1A allele polymorphisms and reproduction may be the most important requirement for yak in the Sarda sheep breed (Carcangiu et al., 2009, survival in this situation. The yak breeding season 2011). Concluding data revealed the positive ef- runs from July to January in China. This period fect of melatonin treatment on the time of the is perfectly synchronized with the long nights first conception in ewe lambs and highlighted that and short days between the summer solstice and +/+ genotype is able to influence reproductive re- winter solstice. sponse to melatonin treatment. Melatonin-treated The pineal gland is the only endocrine organ animals of +/+ genotype showed a higher number that can transform light into endocrine informa- of pregnancies and lambed earlier compared to tion (Binkley, 1993). Melatonin is a polypeptide untreated animals of the same genotype in MTNR1 hormone, which is synthesized primarily in the (Mura et al., 2010). Melatonin secretion cycle pineal gland. The day length is the main factor varied under different lighting conditions (Ogino to initiate the yak breeding season each year via et al., 2013). There is no doubt that melatonin melatonin. Melatonin has an important role in participates in reproduction but the process is the maturation of oocytes where the melatonin not clear. We hypothesized that melatonin may Supported by the National Natural Science Foundation of China (Project No. 31260589). 140 Czech J. Anim. Sci., 59, 2014 (3): 140–145 Original Paper regulate yak reproduction via the hypothalamus- 5 min, 95°C for 10 s, and 60°C for 30 s. The cycle pituitary gland-gonad axis. threshold (Ct) was returned to the baseline dur- In this study, we report the expression of MTNR ing each reaction. Based on the melting curve, we in the pineal gland, hypothalamus, pituitary gland, determined whether a specific product or a primer and ovary of the yak. We also examined differences dimer was present in the PCR during each reaction. in the tissue-specific mRNA expression level of the The standard curves were generated from a stand- MTNR gene in the yak during the breeding season. ard sample, i.e. a 10-fold serial dilution (from 101 to 106). The standard curve parameter calculations MATERIAL AND METHODS were used to determine the correlation coefficient 2 value: R MTNR1A = 0.997, slope = –3.387, intercept = 2 Sample collection and preservation. Tissue 28.833; R MTNR2B = 0.997, slope = –3.417, intercept = 2 samples from the pineal gland, hypothalamus, pi- 29.462; R β-actin = 0.999, slope = –3.389, intercept = tuitary gland, and ovary were obtained at the time 16.654. Each sample was tested in triplicate. of slaughter and stored immediately in RNAlater Immunohistochemical analysis of MTNR pro- (Omega Bio-Tek, Inc., Norcross, USA) and para- tein expression. An immunohistochemical assay formaldehyde until further use. Samples were was developed to study MTNR protein expres- collected from six yaks (proestrus) on October 4, sion in yak tissues (pineal gland, hypothalamus, 2012, which was during the breeding season. pituitary gland, and ovary) during the breeding RNA isolation and reverse transcription-poly- season. The tissues were embedded in paraffin merase chain reaction (RT-PCR). Total tissue and dehydrated. MTNR protein expression was RNA was extracted using RNAiso Plus (TaKaRa analyzed using an SP immunohistochemistry kit Biotechnology Co., Dalian, P.R. China) and the (Maixin, Fuzhou, P.R. China), according to the quality was checked with UV-800 ultraviolet spec- manufacturer’s instructions. trophotometer (Shimadzu Corp., Kyoto, Japan) in Statistical analysis. The data were expressed A260/280 nm. Reverse transcription was performed as the mean ± SD. The SPSS software package using PrimeScript RT Master Mix Perfect Real (Version 15.0, 2007) was used to analyze the data. Time (TaKaRa) in a reaction mixture volume of ANOVA was used to test for significant differences 10 μl at 37°C for 15 min and 85°C for 5 s. between different groups. Real-Time PCR of MTNR mRNA expression. To compare MTNR mRNA expression in different yak RESULTS tissues (pineal gland, hypothalamus, pituitary gland, and ovary) during the breeding season, a real-time Tissue-specific expression of the yak mela- PCR assay was developed based on SXBR Premix tonin receptor during the breeding season. The Ex TaqTM II (Perfect Real Time) (TaKaRa). The MTNR1A and MTNR1B mRNA expression levels β-actin was used as a housekeeping gene to cor- were higher in pineal gland tissue compared with rect potential variations in the RNA loading. The the hypothalamus, pituitary gland, and ovary (P < primers were designed using Primer Premier 6.0 0.01) during the yak breeding season (Figure 1). based on the mRNA sequence of MTNR1B. Tau- rus (NCBI Accession numbers XM614283.3 and 1.2 XM001254949.3). The primers used for MTNR1A 1.0 MT1 MT2 were 5'-GGCACTCGTCATCATTCC-3' (forward) 0.8 and 5'-CGTCCACTCCAGTCTTCT-3' (reverse) 0.6 while those used for MTNR1B were 5'-TCGTC- 0.4 TATGGGCTCCTGAA-3' (forward) and 5'-GCT- 0.2 GCCCTTGGAAGAGTT-3' (reverse). The primers 0.0 used for the β-actin plasmid were 5'-CACAGC- Pineal gland Hypothalamus Pituitary gland Ovary CGAGCGGGAAAT-3' (forward) and 5'-CCGT- GTTGGCGTAGAGGT-3' (reverse) (Zi et al., 2012). Figure 1. MTNR1A and MTNR2B mRNA expression in Real-time PCR conditions: 12.5 μl SXBR Premix pineal gland, hypothalamus, pituitary gland, and ovary Ex TaqTM II (2×), 2.0 μl of template cDNA, 1.0 μl tissue of the yak during breeding season (n = 6) as deter- of each primer (10 μmol/l), 8.5 μl deionized H2O. mined by real-time PCR. Values are normalized with the The PCR parameters were 50°C for 2 min, 95°C for values for β-actin. Each sample was analyzed in triplicate 141 Original Paper Czech J. Anim. Sci., 59, 2014 (3): 140–145 Figure 2. Melatonin receptor protein expressions in pineal Figure 3. Melatonin receptor protein expression in hypo- gland tissue of the yak during breeding season (n = 6) as thalamus issue of the yak during breeding season (n = 6) as determined by immunofluorescence. The pineal gland, determined by immunofluorescence. Melatonin receptor pinealocyte (PC), synaptic ribbon (SR), and synaptic was obviously located in magnocellular neurons (MN) spherules (SS) were the receptors of melatonin and parvicellular neurons (PN) There were no significant differences between the Melatonin receptor protein expression in the hypothalamus, pituitary gland, and ovary tissue. pituitary gland. Low MTNR expression was de- Melatonin receptor protein expression in the tected in the pituitary gland tissue α-cells and pineal gland. The pineal gland is the main tissue β-cells during the yak breeding season (Figure 4). where melatonin was produced. The pinealocyte, Melatonin receptor protein expression in the synaptic ribbon (SR), and synaptic spherules (SS) ovary. In the ovary, MTNR expression was high expressed melatonin in the pineal gland (Figure 2). in the ovarian follicle (Figure 5A) but lower in the This suggests that the pinealocytes exchanged in- corpus luteum (Figure 5B) than in Leydig cells. formation via the SR and SS. Thus, the pinealocytes MTNR expression was detected in granular leu- produced melatonin and they also received it. kocytes and oocytes. This suggests that melatonin Melatonin receptor protein expression in the was involved with the growth and maturation of hypothalamus. High MTNR expression was de- ovarian follicles and it also participated in the tected in the magnocellular neurons and parvicel- growth of oocytes. Melatonin also stimulated lular neurons of the hypothalamus tissue during hormone production by Leydig cells. MTNR was the breeding season (Figure 3). expressed by the granulosa cells in the follicle during each stage. DISCUSSION This study investigated MTNR gene expression in the yak (B. grunniens). We examined tissue- specific differences in the MTNR mRNA expression levels in the yak during the breeding season. We also studied various characteristics of the tissue- specific MTNR protein expression in the yak.
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